diff --git a/Source/Core/Core/Core.cpp b/Source/Core/Core/Core.cpp
index bdd3fcaf10..f1e3161220 100644
--- a/Source/Core/Core/Core.cpp
+++ b/Source/Core/Core/Core.cpp
@@ -21,6 +21,7 @@
 #include "Common/CPUDetect.h"
 #include "Common/CommonPaths.h"
 #include "Common/CommonTypes.h"
+#include "Common/Event.h"
 #include "Common/FileUtil.h"
 #include "Common/Flag.h"
 #include "Common/Logging/LogManager.h"
@@ -110,6 +111,7 @@ struct HostJob
 };
 static std::mutex s_host_jobs_lock;
 static std::queue<HostJob> s_host_jobs_queue;
+static Common::Event s_cpu_thread_job_finished;
 
 static thread_local bool tls_is_cpu_thread = false;
 
@@ -433,6 +435,7 @@ static void EmuThread(std::unique_ptr<BootParameters> boot, WindowSystemInfo wsi
   Common::ScopeGuard movie_guard{Movie::Shutdown};
 
   HW::Init();
+
   Common::ScopeGuard hw_guard{[] {
     // We must set up this flag before executing HW::Shutdown()
     s_hardware_initialized = false;
@@ -771,6 +774,45 @@ void RunAsCPUThread(std::function<void()> function)
     PauseAndLock(false, was_unpaused);
 }
 
+void RunOnCPUThread(std::function<void()> function, bool wait_for_completion)
+{
+  // If the CPU thread is not running, assume there is no active CPU thread we can race against.
+  if (!IsRunning() || IsCPUThread())
+  {
+    function();
+    return;
+  }
+
+  // Pause the CPU (set it to stepping mode).
+  const bool was_running = PauseAndLock(true, true);
+
+  // Queue the job function.
+  if (wait_for_completion)
+  {
+    // Trigger the event after executing the function.
+    s_cpu_thread_job_finished.Reset();
+    CPU::AddCPUThreadJob([&function]() {
+      function();
+      s_cpu_thread_job_finished.Set();
+    });
+  }
+  else
+  {
+    CPU::AddCPUThreadJob(std::move(function));
+  }
+
+  // Release the CPU thread, and let it execute the callback.
+  PauseAndLock(false, was_running);
+
+  // If we're waiting for completion, block until the event fires.
+  if (wait_for_completion)
+  {
+    // Periodically yield to the UI thread, so we don't deadlock.
+    while (!s_cpu_thread_job_finished.WaitFor(std::chrono::milliseconds(10)))
+      Host_YieldToUI();
+  }
+}
+
 // Display FPS info
 // This should only be called from VI
 void VideoThrottle()
diff --git a/Source/Core/Core/Core.h b/Source/Core/Core/Core.h
index fdd30a539a..26e30a2d8a 100644
--- a/Source/Core/Core/Core.h
+++ b/Source/Core/Core/Core.h
@@ -82,6 +82,10 @@ void UpdateTitle();
 // This should only be called from the CPU thread or the host thread.
 void RunAsCPUThread(std::function<void()> function);
 
+// Run a function on the CPU thread, asynchronously.
+// This is only valid to call from the host thread, since it uses PauseAndLock() internally.
+void RunOnCPUThread(std::function<void()> function, bool wait_for_completion);
+
 // for calling back into UI code without introducing a dependency on it in core
 using StateChangedCallbackFunc = std::function<void(Core::State)>;
 void SetOnStateChangedCallback(StateChangedCallbackFunc callback);
diff --git a/Source/Core/Core/HW/CPU.cpp b/Source/Core/Core/HW/CPU.cpp
index a1b21ea7a2..b8243a0452 100644
--- a/Source/Core/Core/HW/CPU.cpp
+++ b/Source/Core/Core/HW/CPU.cpp
@@ -6,6 +6,7 @@
 
 #include <condition_variable>
 #include <mutex>
+#include <queue>
 
 #include "AudioCommon/AudioCommon.h"
 #include "Common/CommonTypes.h"
@@ -44,6 +45,7 @@ static bool s_state_paused_and_locked = false;
 static bool s_state_system_request_stepping = false;
 static bool s_state_cpu_step_instruction = false;
 static Common::Event* s_state_cpu_step_instruction_sync = nullptr;
+static std::queue<std::function<void()>> s_pending_jobs;
 
 void Init(PowerPC::CPUCore cpu_core)
 {
@@ -60,6 +62,9 @@ void Shutdown()
 // Requires holding s_state_change_lock
 static void FlushStepSyncEventLocked()
 {
+  if (!s_state_cpu_step_instruction)
+    return;
+
   if (s_state_cpu_step_instruction_sync)
   {
     s_state_cpu_step_instruction_sync->Set();
@@ -68,12 +73,25 @@ static void FlushStepSyncEventLocked()
   s_state_cpu_step_instruction = false;
 }
 
+static void ExecutePendingJobs(std::unique_lock<std::mutex>& state_lock)
+{
+  while (!s_pending_jobs.empty())
+  {
+    auto callback = s_pending_jobs.front();
+    s_pending_jobs.pop();
+    state_lock.unlock();
+    callback();
+    state_lock.lock();
+  }
+}
+
 void Run()
 {
   std::unique_lock<std::mutex> state_lock(s_state_change_lock);
   while (s_state != State::PowerDown)
   {
     s_state_cpu_cvar.wait(state_lock, [] { return !s_state_paused_and_locked; });
+    ExecutePendingJobs(state_lock);
 
     switch (s_state)
     {
@@ -108,8 +126,10 @@ void Run()
 
     case State::Stepping:
       // Wait for step command.
-      s_state_cpu_cvar.wait(state_lock,
-                            [] { return s_state_cpu_step_instruction || !IsStepping(); });
+      s_state_cpu_cvar.wait(state_lock, [&state_lock] {
+        ExecutePendingJobs(state_lock);
+        return s_state_cpu_step_instruction || !IsStepping();
+      });
       if (!IsStepping())
       {
         // Signal event if the mode changes.
@@ -330,4 +350,11 @@ bool PauseAndLock(bool do_lock, bool unpause_on_unlock, bool control_adjacent)
   }
   return was_unpaused;
 }
+
+void AddCPUThreadJob(std::function<void()> function)
+{
+  std::unique_lock<std::mutex> state_lock(s_state_change_lock);
+  s_pending_jobs.push(std::move(function));
+}
+
 }  // namespace CPU
diff --git a/Source/Core/Core/HW/CPU.h b/Source/Core/Core/HW/CPU.h
index 408b82ace2..26ffa6783c 100644
--- a/Source/Core/Core/HW/CPU.h
+++ b/Source/Core/Core/HW/CPU.h
@@ -3,6 +3,7 @@
 // Refer to the license.txt file included.
 
 #pragma once
+#include <functional>
 
 namespace Common
 {
@@ -74,4 +75,8 @@ const State* GetStatePtr();
 // "control_adjacent" causes PauseAndLock to behave like EnableStepping by modifying the
 //   state of the Audio and FIFO subsystems as well.
 bool PauseAndLock(bool do_lock, bool unpause_on_unlock = true, bool control_adjacent = false);
+
+// Adds a job to be executed during on the CPU thread. This should be combined with PauseAndLock(),
+// as while the CPU is in the run loop, it won't execute the function.
+void AddCPUThreadJob(std::function<void()> function);
 }  // namespace CPU